Skip to main content
SpringerLink
Log in

The Functions of Pex11 Family Proteins in Peroxisome Biology

  • Chapter
  • First Online:
Molecular Machines Involved in Peroxisome Biogenesis and Maintenance

  • 873 Accesses

Abstract

Regulating peroxisome numbers within the cell, through synthesis and degradation events, is an essential part of cell homeostasis. New peroxisomes are made either de novo or by the division of pre-existing organelles. Elongation of the peroxisomal membrane, one of the initial steps in fission, is proposed to be followed by assembly of the membrane fission machinery at the site of tubulation, bilayer constriction and ultimately, membrane fission. A role for the peroxisomal membrane protein Pex11p in peroxisome fission has long been known. Recent reports have shed light on the mechanistic details behind Pex11p’s membrane remodeling activity and the role of amphipathic helices in Pex11p. However, a number of additional tasks have been attributed to Pex11p, ranging from directing peroxisome inheritance to peroxisomal membrane protein reorganization. Furthermore, several Pex11-like proteins have been described, the functions of which differ from Pex11p. This chapter will discuss the current understanding of the role of the Pex11 protein family in peroxisome biogenesis.

This is a preview of subscription content, log in via an institution to check access.

Access this chapter

Log in via an institution
Chapter
USD 29.95
Price excludes VAT (USA)
  • Available as PDF
  • Read on any device
  • Instant download
  • Own it forever
eBook
USD 129.00
Price excludes VAT (USA)
  • Available as EPUB and PDF
  • Read on any device
  • Instant download
  • Own it forever
Softcover Book
USD 169.99
Price excludes VAT (USA)
  • Compact, lightweight edition
  • Dispatched in 3 to 5 business days
  • Free shipping worldwide - see info
Hardcover Book
USD 169.99
Price excludes VAT (USA)
  • Durable hardcover edition
  • Dispatched in 3 to 5 business days
  • Free shipping worldwide - see info

Tax calculation will be finalised at checkout

Purchases are for personal use only

Institutional subscriptions

References

  • Abe I, Okumoto K, Tamura S, Fujiki Y (1998) Clofibrate-inducible, 28-kDa peroxisomal integral membrane protein is encoded by PEX11. FEBS Lett 431:468–472

    Article  CAS  PubMed  Google Scholar 

  • Anton M, Passreiter M, Lay D, Thai TP, Gorgas K, Just WW (2000) ARF- and coatomer-mediated peroxisomal vesiculation. Cell Biochem Biophys 32:27–36

    Article  PubMed  Google Scholar 

  • Bleazard W, Mccaffery JM, King EJ, Bale S, Mozdy A, Tieu Q, Nunnari J, Shaw JM (1999) The dynamin-related GTPase Dnm1 regulates mitochondrial fission in yeast. Nat Cell Biol 1:298–304

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  • Cepinska MN, Veenhuis M, Van Der Klei IJ, Nagotu S (2011) Peroxisome fission is associated with reorganization of specific membrane proteins. Traffic 12:925–937

    Article  CAS  PubMed  Google Scholar 

  • Cosson P, Letourneur F (1994) Coatomer interaction with di-lysine endoplasmic reticulum retention motifs. Science 263:1629–1631

    Article  CAS  PubMed  Google Scholar 

  • Cosson P, Letourneur F (1997) Coatomer (COPI)-coated vesicles: role in intracellular transport and protein sorting. Curr Opin Cell Biol 9:484–487

    Article  CAS  PubMed  Google Scholar 

  • Desai M, Hu J (2008) Light induces peroxisome proliferation in Arabidopsis seedlings through the photoreceptor phytochrome A, the transcription factor HY5 HOMOLOG, and the peroxisomal protein PEROXIN11b. Plant Physiol 146:1117–1127

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  • Distel B, Erdmann R, Gould SJ, Blobel G, Crane DI, Cregg JM, Dodt G, Fujiki Y, Goodman JM, Just WW, Kiel JA, Kunau WH, Lazarow PB, Mannaerts GP, Moser HW, Osumi T, Rachubinski RA, Roscher A, Subramani S, Tabak HF, Tsukamoto T, Valle D, Van Der Klei I, Van Veldhoven PP, Veenhuis M (1996) A unified nomenclature for peroxisome biogenesis factors. J Cell Biol 135:1–3

    Article  CAS  PubMed  Google Scholar 

  • Ebberink MS, Koster J, Visser G, Spronsen F, Stolte-Dijkstra I, Smit GP, Fock JM, Kemp S, Wanders RJ, Waterham HR (2012) A novel defect of peroxisome division due to a homozygous non-sense mutation in the PEX11beta gene. J Med Genet 49:307–313

    Article  CAS  PubMed  Google Scholar 

  • Erdmann R, Blobel G (1995) Giant peroxisomes in oleic acid-induced Saccharomyces cerevisiae lacking the peroxisomal membrane protein Pmp27p. J Cell Biol 128:509–523

    Article  CAS  PubMed  Google Scholar 

  • Fagarasanu A, Fagarasanu M, Rachubinski RA (2007) Maintaining peroxisome populations: a story of division and inheritance. Annu Rev Cell Dev Biol 23:321–344

    Article  CAS  PubMed  Google Scholar 

  • Gandre-Babbe S, Van Der Bliek AM (2008) The novel tail-anchored membrane protein Mff controls mitochondrial and peroxisomal fission in mammalian cells. Mol Biol Cell 19:2402–2412

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  • Gurvitz A, Rottensteiner H (2006) The biochemistry of oleate induction: transcriptional upregulation and peroxisome proliferation. Biochim Biophys Acta 1763:1392–1402

    Article  CAS  PubMed  Google Scholar 

  • Gurvitz A, Hiltunen JK, Erdmann R, Hamilton B, Hartig A, Ruis H, Rottensteiner H (2001) Saccharomyces cerevisiae Adr1p governs fatty acid beta-oxidation and peroxisome proliferation by regulating POX1 and PEX11. J Biol Chem 276:31825–31830

    Article  CAS  PubMed  Google Scholar 

  • Huber A, Koch J, Kragler F, Brocard C, Hartig A (2012) A subtle interplay between three Pex11 proteins shapes de novo formation and fission of peroxisomes. Traffic 13:157–167

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  • Joshi S, Agrawal G, Subramani S (2012) Phosphorylation-dependent Pex11p and Fis1p interaction regulates peroxisome division. Mol Biol Cell 23:1307–1315

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  • Kiel JA, Van Der Klei IJ, Van Den Berg MA, Bovenberg RA, Veenhuis M (2005) Overproduction of a single protein, Pc-Pex11p, results in 2-fold enhanced penicillin production by Penicillium chrysogenum. Fungal Genet Biol 42:154–164

    Article  CAS  PubMed  Google Scholar 

  • Kiel JA, Veenhuis M, Van Der Klei IJ (2006) PEX genes in fungal genomes: common, rare or redundant. Traffic 7:1291–1303

    Article  CAS  PubMed  Google Scholar 

  • Knoblach B, Rachubinski RA (2010) Phosphorylation-dependent activation of peroxisome proliferator protein PEX11 controls peroxisome abundance. J Biol Chem 285:6670–6680

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  • Kobayashi S, Tanaka A, Fujiki Y (2007) Fis1, DLP1, and Pex11p coordinately regulate peroxisome morphogenesis. Exp Cell Res 313:1675–1686

    Article  CAS  PubMed  Google Scholar 

  • Koch J, Brocard C (2011) Membrane elongation factors in organelle maintenance: the case of peroxisome proliferation. Biomol Concepts 2:353–364

    CAS  PubMed Central  PubMed  Google Scholar 

  • Koch J, Brocard C (2012) PEX11 proteins attract Mff and human Fis1 to coordinate peroxisomal fission. J Cell Sci 125:3813–3826

    Article  CAS  PubMed  Google Scholar 

  • Koch A, Schneider G, Luers GH, Schrader M (2004) Peroxisome elongation and constriction but not fission can occur independently of dynamin-like protein 1. J Cell Sci 117:3995–4006

    Article  CAS  PubMed  Google Scholar 

  • Koch J, Pranjic K, Huber A, Ellinger A, Hartig A, Kragler F, Brocard C (2010) PEX11 family members are membrane elongation factors that coordinate peroxisome proliferation and maintenance. J Cell Sci 123:3389–3400

    Article  CAS  PubMed  Google Scholar 

  • Krikken AM, Veenhuis M, Van Der Klei IJ (2009) Hansenula polymorpha pex11 cells are affected in peroxisome retention. FEBS J 276:1429–1439

    Article  CAS  PubMed  Google Scholar 

  • Kurbatova E, Otzen M, Van Der Klei IJ (2009) p24 proteins play a role in peroxisome proliferation in yeast. FEBS Lett 583:3175–3180

    Article  CAS  PubMed  Google Scholar 

  • Li X, Gould SJ (2002) PEX11 promotes peroxisome division independently of peroxisome metabolism. J Cell Biol 156:643–651

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  • Li X, Gould SJ (2003) The dynamin-like GTPase DLP1 is essential for peroxisome division and is recruited to peroxisomes in part by PEX11. J Biol Chem 278:17012–17020

    Article  CAS  PubMed  Google Scholar 

  • Li X, Baumgart E, Dong GX, Morrell JC, Jimenez-Sanchez G, Valle D, Smith KD, Gould SJ (2002a) PEX11alpha is required for peroxisome proliferation in response to 4-phenylbutyrate but is dispensable for peroxisome proliferator-activated receptor alpha-mediated peroxisome proliferation. Mol Cell Biol 22:8226–8240

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  • Li X, Baumgart E, Morrell JC, Jimenez-Sanchez G, Valle D, Gould SJ (2002b) PEX11 beta deficiency is lethal and impairs neuronal migration but does not abrogate peroxisome function. Mol Cell Biol 22:4358–4365

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  • Lingard MJ, Trelease RN (2006) Five Arabidopsis peroxin 11 homologs individually promote peroxisome elongation, duplication or aggregation. J Cell Sci 119:1961–1972

    Article  CAS  PubMed  Google Scholar 

  • Lingard MJ, Gidda SK, Bingham S, Rothstein SJ, Mullen RT, Trelease RN (2008) Arabidopsis PEROXIN11c-e, FISSION1b, and DYNAMIN-RELATED PROTEIN3A cooperate in cell cycle-associated replication of peroxisomes. Plant Cell 20:1567–1585

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  • Lorenz P, Maier AG, Baumgart E, Erdmann R, Clayton C (1998) Elongation and clustering of glycosomes in Trypanosoma brucei overexpressing the glycosomal Pex11p. EMBO J 17:3542–3555

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  • Lorenz H, Hailey DW, Wunder C, Lippincott-Schwartz J (2006) The fluorescence protease protection (FPP) assay to determine protein localization and membrane topology. Nat Protoc 1:276–279

    Article  CAS  PubMed  Google Scholar 

  • Low C, Weininger U, Lee H, Schweimer K, Neundorf I, Beck-Sickinger AG, Pastor RW, Balbach J (2008) Structure and dynamics of helix-0 of the N-BAR domain in lipid micelles and bilayers. Biophys J 95:4315–4323

    Article  PubMed Central  PubMed  Google Scholar 

  • Maier AG, Schulreich S, Bremser M, Clayton C (2000) Binding of coatomer by the PEX11 C-terminus is not required for function. FEBS Lett 484:82–86

    Article  CAS  PubMed  Google Scholar 

  • Maier A, Lorenz P, Voncken F, Clayton C (2001) An essential dimeric membrane protein of trypanosome glycosomes. Mol Microbiol 39:1443–1451

    Article  CAS  PubMed  Google Scholar 

  • Marshall PA, Krimkevich YI, Lark RH, Dyer JM, Veenhuis M, Goodman JM (1995) Pmp27 promotes peroxisomal proliferation. J Cell Biol 129:345–355

    Article  CAS  PubMed  Google Scholar 

  • Marshall PA, Dyer JM, Quick ME, Goodman JM (1996) Redox-sensitive homodimerization of Pex11p: a proposed mechanism to regulate peroxisomal division. J Cell Biol 135:123–137

    Article  CAS  PubMed  Google Scholar 

  • Mears JA, Lackner LL, Fang S, Ingerman E, Nunnari J, Hinshaw JE (2011) Conformational changes in Dnm1 support a contractile mechanism for mitochondrial fission. Nat Struct Mol Biol 18:20–26

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  • Motley AM, Hettema EH (2007) Yeast peroxisomes multiply by growth and division. J Cell Biol 178:399–410

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  • Motley AM, Ward GP, Hettema EH (2008) Dnm1p-dependent peroxisome fission requires Caf4p, Mdv1p and Fis1p. J Cell Sci 121:1633–1640

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  • Mozdy AD, Mccaffery JM, Shaw JM (2000) Dnm1p GTPase-mediated mitochondrial fission is a multi-step process requiring the novel integral membrane component Fis1p. J Cell Biol 151:367–380

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  • Nagotu S, Saraya R, Otzen M, Veenhuis M, Van Der Klei IJ (2008) Peroxisome proliferation in Hansenula polymorpha requires Dnm1p which mediates fission but not de novo formation. Biochim Biophys Acta 1783:760–769

    Article  CAS  PubMed  Google Scholar 

  • Nayidu NK, Wang L, Xie W, Zhang C, Fan C, Lian X, Zhang Q, Xiong L (2008) Comprehensive sequence and expression profile analysis of PEX11 gene family in rice. Gene 412:59–70

    Article  CAS  PubMed  Google Scholar 

  • Opalinski L, Kiel JA, Williams C, Veenhuis M, Van Der Klei IJ (2010) Membrane curvature during peroxisome fission requires Pex11. EMBO J 30:5–16

    Article  PubMed Central  PubMed  Google Scholar 

  • Opalinski L, Bartoszewska M, Fekken S, Liu H, De Boer R, Van Der Klei I, Veenhuis M, Kiel JA (2012) De novo peroxisome biogenesis in Penicillium chrysogenum is not dependent on the Pex11 family members or Pex16. PLoS One 7:e35490

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  • Orth T, Reumann S, Zhang X, Fan J, Wenzel D, Quan S, Hu J (2007) The PEROXIN11 protein family controls peroxisome proliferation in Arabidopsis. Plant Cell 19:333–350

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  • Otera H, Wang C, Cleland MM, Setoguchi K, Yokota S, Youle RJ, Mihara K (2010) Mff is an essential factor for mitochondrial recruitment of Drp1 during mitochondrial fission in mammalian cells. J Cell Biol 191:1141–1158

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  • Otsuga D, Keegan BR, Brisch E, Thatcher JW, Hermann GJ, Bleazard W, Shaw JM (1998) The dynamin-related GTPase, Dnm1p, controls mitochondrial morphology in yeast. J Cell Biol 143:333–349

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  • Passreiter M, Anton M, Lay D, Frank R, Harter C, Wieland FT, Gorgas K, Just WW (1998) Peroxisome biogenesis: involvement of ARF and coatomer. J Cell Biol 141:373–383

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  • Rottensteiner H, Kal AJ, Filipits M, Binder M, Hamilton B, Tabak HF, Ruis H (1996) Pip2p: a transcriptional regulator of peroxisome proliferation in the yeast Saccharomyces cerevisiae. EMBO J 15:2924–2934

    CAS  PubMed Central  PubMed  Google Scholar 

  • Rottensteiner H, Hartig A, Hamilton B, Ruis H, Erdmann R, Gurvitz A (2003a) Saccharomyces cerevisiae Pip2p-Oaf1p regulates PEX25 transcription through an adenine-less ORE. Eur J Biochem 270:2013–2022

    Article  CAS  PubMed  Google Scholar 

  • Rottensteiner H, Stein K, Sonnenhol E, Erdmann R (2003b) Conserved function of pex11p and the novel pex25p and pex27p in peroxisome biogenesis. Mol Biol Cell 14:4316–4328

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  • Sakai Y, Marshall PA, Saiganji A, Takabe K, Saiki H, Kato N, Goodman JM (1995) The Candida boidinii peroxisomal membrane protein Pmp30 has a role in peroxisomal proliferation and is functionally homologous to Pmp27 from Saccharomyces cerevisiae. J Bacteriol 177:6773–6781

    CAS  PubMed Central  PubMed  Google Scholar 

  • Saraya R, Krikken AM, Veenhuis M, Van Der Klei IJ (2011) Peroxisome reintroduction in Hansenula polymorpha requires Pex25 and Rho1. J Cell Biol 193:885–900

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  • Schrader M, Krieglstein K, Fahimi HD (1998a) Tubular peroxisomes in HepG2 cells: selective induction by growth factors and arachidonic acid. Eur J Cell Biol 75:87–96

    Article  CAS  PubMed  Google Scholar 

  • Schrader M, Reuber BE, Morrell JC, Jimenez-Sanchez G, Obie C, Stroh TA, Valle D, Schroer TA, Gould SJ (1998b) Expression of PEX11beta mediates peroxisome proliferation in the absence of extracellular stimuli. J Biol Chem 273:29607–29614

    Article  CAS  PubMed  Google Scholar 

  • Schrader M, Almeida M, Grille S (2012a) Postfixation detergent treatment liberates the membrane modelling protein Pex11beta from peroxisomal membranes. Histochem Cell Biol 138:541–547

    Article  CAS  PubMed  Google Scholar 

  • Schrader M, Bonekamp NA, Islinger M (2012b) Fission and proliferation of peroxisomes. Biochim Biophys Acta 1822:1343–1357

    Article  CAS  PubMed  Google Scholar 

  • Shimizu M, Akter MH, Emi Y, Sato R, Yamaguchi T, Hirose F, Osumi T (2006) Peroxisome proliferator-activated receptor subtypes differentially cooperate with other transcription factors in selective transactivation of the perilipin/PEX11 alpha gene pair. J Biochem 139:563–573

    Article  CAS  PubMed  Google Scholar 

  • Smith JJ, Marelli M, Christmas RH, Vizeacoumar FJ, Dilworth DJ, Ideker T, Galitski T, Dimitrov K, Rachubinski RA, Aitchison JD (2002) Transcriptome profiling to identify genes involved in peroxisome assembly and function. J Cell Biol 158:259–271

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  • Tam YY, Torres-Guzman JC, Vizeacoumar FJ, Smith JJ, Marelli M, Aitchison JD, Rachubinski RA (2003) Pex11-related proteins in peroxisome dynamics: a role for the novel peroxin Pex27p in controlling peroxisome size and number in Saccharomyces cerevisiae. Mol Biol Cell 14:4089–4102

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  • Thoms S, Erdmann R (2005) Dynamin-related proteins and Pex11 proteins in peroxisome division and proliferation. FEBS J 272:5169–5181

    Article  CAS  PubMed  Google Scholar 

  • Van Roermund CW, Tabak HF, Van Den Berg M, Wanders RJ, Hettema EH (2000) Pex11p plays a primary role in medium-chain fatty acid oxidation, a process that affects peroxisome number and size in Saccharomyces cerevisiae. J Cell Biol 150:489–498

    Article  PubMed Central  PubMed  Google Scholar 

  • Van Zutphen T, Baerends RJ, Susanna KA, De Jong A, Kuipers OP, Veenhuis M, Van Der Klei IJ (2010) Adaptation of Hansenula polymorpha to methanol: a transcriptome analysis. BMC Genomics 11:1

    Article  PubMed Central  PubMed  Google Scholar 

  • Wieland F, Harter C (1999) Mechanisms of vesicle formation: insights from the COP system. Curr Opin Cell Biol 11:440–446

    Article  CAS  PubMed  Google Scholar 

  • Yoon Y, Krueger EW, Oswald BJ, Mcniven MA (2003) The mitochondrial protein hFis1 regulates mitochondrial fission in mammalian cells through an interaction with the dynamin-like protein DLP1. Mol Cell Biol 23:5409–5420

    Article  CAS  PubMed Central  PubMed  Google Scholar 

Download references

Acknowledgments

CW is supported by a grant from the Netherlands Organization for Scientific research (NWO), section Earth and Life Sciences.

Author information

Authors and Affiliations

  1. Molecular Cell Biology, Groningen Biomolecular Sciences and Biotechnology Institute (GBB), University of Groningen, 9700 CC, Groningen, The Netherlands

    Chris Williams & Ida J. van der Klei

Authors
  1. Chris Williams
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Ida J. van der Klei
    View author publications

    You can also search for this author in PubMed Google Scholar

Corresponding author

Correspondence to Chris Williams .

Editor information

Editors and Affiliations

  1. Mauerbach, Austria

    Cecile Brocard

  2. Max F. Perutz Laboratories University of Vienna, Vienna, Austria

    Andreas Hartig

Rights and permissions

Reprints and permissions

Copyright information

© 2014 Springer-Verlag Wien

About this chapter

Cite this chapter

Williams, C., van der Klei, I.J. (2014). The Functions of Pex11 Family Proteins in Peroxisome Biology. In: Brocard, C., Hartig, A. (eds) Molecular Machines Involved in Peroxisome Biogenesis and Maintenance. Springer, Vienna. https://doi.org/10.1007/978-3-7091-1788-0_19

Download citation

Publish with us

Policies and ethics

Search

Navigation